The natural world is an intricate web of interactions among species. All organisms must avoid enemies, attract mutualists, and acquire enough resources to survive and reproduce. An overarching goal of research in the Whitehead Lab is to understand the ecological mechanisms and evolutionary consequences of these multi-species interactions. We are particularly fascinated with the diverse mixtures of secondary metabolites produced in plants and their critical roles as mediators of both antagonistic and mutualistic interactions with other organisms. We use integrative approaches that utilize modern tools in analytical organic chemistry along with observational field studies, behavioral experiments, and laboratory bioassays.

CURRENT PROJEC﻿TS:

1) Plant evolutionary responses to multi-species interactionsPlants in natural communities interact simultaneously with a diversity of antagonists and mutualists, and thus evolutionary responses to one organism may be constrained by how those responses affect interactions with other organisms. However, we still know very little about how plants evolve in response to multi-species interactions. Our lab is particularly interested in plant defense traits and we are investigating a number of questions that explore the multiple trade-offs involved in defense trait evolution. Does the need to attract mutualists (e.g. seed dispersers or pollinators) constrain the evolution of plant traits that defend against antagonists? How about the reverse? And do selective pressures from one antagonist constrain the defense strategies employed against another? We use a variety of approaches to understand these trade-offs, including: 1) phylogenetic comparative studies across groups of plants that experience variable selective pressures from mutualists and antagonists, and 2) experimental evolution studies that manipulate plant interactions in a controlled fashion across multiple generations.

2) Chemical ecology of seed dispersal and fruit defense

Fleshy fruits function primarily to attract animal seed dispersers, yet they are much more than packages of nutritional rewards. Fruits contain a rich array of secondary metabolites that give them their incredible diversity of flavors, odors, and colors. Some of these metabolites may function as attractants, but many wild fruits also contain metabolites that are deterrent or even highly toxic. In fact, the levels of toxins in fruits can often exceed those in vegetative tissues. Why would a structure that functions to attract mutualists contain toxins? Our research is addressing this evolutionary paradox using secondary metabolites produced in fruits of the tropical plant genus Piper as a model system. This research has involved: 1) working collaboratively with chemists to provide structural elucidation of secondary metabolites in Piper fruit, 2) examining the effects of secondary metabolites on fruit defense through bioassays with insect seed predators and fungal pathogens, and 3) examining the effects of secondary metabolites on seed dispersal through experiments with short-tailed fruit bats (Carollia spp.), the primary seed dispersers of Piper. Together, this body of work has suggested that fruit secondary metabolites represent an adaptive trade-off between the attraction of seed dispersers and defense. However, the strength of this trade-off and its consequences for plant fitness are complex and depend on the community context. We are continuing to explore how fruit secondary metabolites affect multiple aspects of the seed dispersal process and can also have broader consequences in ecological communities by affecting the physiology, immunity, and microbiome of fruit consumers. Collaborators: Deane Bowers, Lee Dyer, Chris Jeffrey, Justin Baldwin, Maria Obando, SeJin Song

3) Domestication and plant defenseSince the beginning of domestication ~10,000 years ago, most crops have been subject to strong selection for traits that are favorable to humans. Does this process inherently lead to plants that are less well-defended against pests? Increased yield of edible biomass is probably the most important driving force in agronomic selection, and plant resource allocation theory suggests that the resources necessary to increase biomass will be diverted from other metabolically costly processes, such as the production of chemical or physical defenses. We are working collaboratively on several projects to understand broad patters of plant defense evolution under domestication. First, we have compiled a large database of published studies that compare plant defense or herbivore resistance among crops and their wild relatives. We are using phylogenetically-controlled meta-analyses to test how the evolution of defense traits during domestication depends on a variety of factors. Second, we are using apples and their insect herbivores as a model system to understand how domestication, and particularly selection for increased yield, can influence plant defense. Using field observations, bioassays, and analyses of secondary metabolites across 108 wild and domestic apple genotypes, our work has shown that high-yielding domestic apple varieties produce lower concentrations of defensive metabolites and have altered interactions with herbivores. This suggests that selection for increased yield can result in allocation trade-offs that reduce investment in plant defense.

4) Agricultural applications of chemical ecologyThere are numerous success stories that demonstrate how an improved understanding of the mechanisms of plant defense can lead to novel tools for pest management that increase agricultural sustainability. We are working to contribute to this field by investigating the chemical mechanisms of interactions between apples and their insect herbivores. Apples are one of the fruit crops most heavily attacked by insect pests, requiring intensive management to produce economically-viable crop yields. We are examining: 1) how the diversity of phenolic metabolites in fruit skin and pulp function in fruit defense, and 2) how fruit defenses are induced by insect damage and whether these responses can be manipulated with phytohormones to reduce insect damage in orchards. ﻿Collaborators:Katja Poveda and Art Agnello